Advertisement

Comparative analysis of glucose metabolism responses of large yellow croaker Larimichthys crocea fed diet with fish oil and palm oil

  • Qi Wang
  • Hua Mu
  • Haohao Shen
  • Zhixiang Gu
  • Dong Liu
  • Mengxi Yang
  • Yue Zhang
  • Weiqi Xu
  • Wenbing ZhangEmail author
  • Kangsen Mai
Article

Abstract

In order to study the effects of dietary fatty acid compositions on glucose metabolism, large yellow croaker juveniles Larimichthys crocea (initial weight, 36.80 ± 0.39 g) were fed with two experiment diets for 12 weeks. The two diets contained 6.5% of fish oil (FO) and palm oil (PO), respectively. Results showed that the contents of saturated fatty acids in liver and muscle, levels of glucose, triglyceride (TG), non-esterified fatty acid (NEFA), and leptin in blood were significantly higher in PO group, while the hepatic glycogen and muscle glycogen significantly decreased (P < 0.05). There were no significant differences in blood insulin and adiponectin levels between the two groups (P > 0.05). Compared with the FO group, the expressions of glucokinase (GK), glucose-6-phosphate dehydrogenase, glycogen synthase (GYS), glucose transporter 2 (GLUT2), insulin receptor 1 (IR1), insulin receptor substrate 1 (IRS1), insulin receptor substrate (IRS2), and protein kinase B (AKT2) were significantly decreased, and the expressions of phosphoenolpyruvate carboxykinase (PEPCK) in liver were significantly increased in the PO group. Meanwhile, the expressions of GK, phosphofructokinase, GYS, GLUT4, and insulin receptor 2 (IR2) were significantly reduced, and the expressions PEPCK, fructose-1 and 6-diphosphatase in muscle were significantly increased in the PO group. In conclusion, palm oil in diet could inhibit the utilization of glucose and promote the endogenous glucose production in large yellow croaker by reducing the sensitivity of insulin, so as to increase the blood glucose level.

Keywords

Large yellow croaker Fish oil Palm oil Gene expression Glucose metabolism 

Notes

Funding

This work was financially supported by the National Natural Science Foundation of China (Grant No. 31572628) and the Fundamental Research Funds for the Central Universities of Ocean University of China (No. 201562017).

References

  1. Aguilar AJ, CondeSieira M, Polakof S, Míguez JM, Soengas JL (2010) Central leptin treatment modulates brain glucosensing function and peripheral energy metabolism of rainbow trout. Peptides 31(6):1044–1054Google Scholar
  2. Amelsvoort JMMV, Beek AVD, Stam JJ (1986) Effects of the type of dietary fatty acid on the insulin receptor function in rat epididymal fat cells. Ann Nutr Metab 30(4):273–280Google Scholar
  3. Banks WA, Coon AB, Robinson SM, Asif M, Shultz JM, Ryota N, Morley JE (2004) Triglycerides induce leptin resistance at the blood-brain barrier. Diabetes 53(5):1253–1260Google Scholar
  4. Babaei S, Abedian KA, Hedayati M, Yazdani M A (2017) Growth response, body composition, plasma metabolites, digestive and antioxidant enzymes activities of Siberian sturgeon (Acipenser baerii, Brandt, 1869) fed different dietary protein and carbohydrate, lipid ratio. Aquaclture Research 48: 2642-2654Google Scholar
  5. Bell JG, Henderson RJ, Tocher DR, Mcghee F, Dick JR, Porter A, Smullen RP, Sargent JR (2002) Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects muscle fatty acid composition and hepatic fatty acid metabolism. J Nutr 132(2):222–230Google Scholar
  6. Berg AH, Combs TP, Scherer PE (2002) ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab 13(2):84–89Google Scholar
  7. Boden G, Chen X, Ruiz J, White JV, Rossetti L (1994) Mechanisms of fatty acid-induced inhibition of glucose uptake. J Clin Investig 93(6):2438–2446Google Scholar
  8. Brekke HK, Lenner RA, Taskinen MR, Månsson JE, Funahashi T, Matsuzawa Y, Jansson PA (2005) Lifestyle modification improves risk factors in type 2 diabetes relatives. Diabetes Res Clin Pract 68(1):18–28Google Scholar
  9. Bueno AA, Oyama LM, De OC, Pisani LP, Ribeiro EB, Silveira VL, Cm ODN (2008) Effects of different fatty acids and dietary lipids on adiponectin gene expression in 3T3-L1 cells and C57BL/6J mice adipose tissue. Pflugers Arch-Eur J Physiol 455(4):701–709Google Scholar
  10. Ceddia RB, Lopes G, Souza HM, Borba-Murad GR, William WN, Bazotte RB, Curi R (1999a) Acute effects of leptin on glucose metabolism of in situ rat perfused livers and isolated hepatocytes. Int J Obes 23(11):1207–1212Google Scholar
  11. Ceddia RB, William WN, Carpinelli AR et al (1999b) Modulation of insulin secretion by leptin. Gen Pharmacol 32(2):233–237Google Scholar
  12. Chen NG, Swick AG, Romsos DR (1997) Leptin constrains acetylcholine-induced insulin secretion from pancreatic islets of ob/ob mice. J Clin Investig 100(5):1174–1179Google Scholar
  13. Cheng L, Yu Y, Szabo A, Wu Y, Wang H, Camer D, Huang XF (2015) Palmitic acid induces central leptin resistance and impairs hepatic glucose and lipid metabolism in male mice. J Nutr Biochem 26(5):541–548Google Scholar
  14. Chunli Y, Yan C, Cline GW, Dongyan Z, Haihong Z, Yanlin W, Raynald B, Kim JK, Cushman SW, Cooney GJ (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem 277(52):50230–50236Google Scholar
  15. Coccia E, Varricchio E, Vito P, Turchini GM, Francis DS, Paolucci M (2014) Fatty acid-specific alterations in leptin, PPARα, and CPT-1 gene expression in the rainbow trout. Lipids 49(10):1033–1046Google Scholar
  16. Emilsson V, Liu YL, Cawthorne MA, Morton NM, Davenport M (1997) Expression of the functional leptin receptor mRNA in pancreatic islets and direct inhibitory action of leptin on insulin secretion. Diabetes 46(2):313–316Google Scholar
  17. Flachs P, Mohamedali V, Horakova O, Rossmeisl M, Hosseinzadehattar MJ, Hensler M, Ruzickova J, Kopecky J (2006) Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed a high-fat diet. Diabetologia 49(2):394–397Google Scholar
  18. Fountoulaki E, Vasilaki A, Hurtado R, Grigorakis K, Karacostas I, Nengas I, Rigos G, Kotzamanis Y, Venou B, Alexis MN (2009) Fish oil substitution by vegetable oils in commercial diets for gilthead sea bream (Sparus aurata L.); effects on growth performance, flesh quality and fillet fatty acid profile: recovery of fatty acid profiles by a fish oil finishing diet under fluctuating water temperatures. Aquaculture 289(3):317–326Google Scholar
  19. Ishii M, Maeda A, Tani S, Akagawa M (2015) Palmitate induces insulin resistance in human HepG2 hepatocytes by enhancing ubiquitination and proteasomal degradation of key insulin signaling molecules. Arch Biochem Biophys 566(11):26–35Google Scholar
  20. Kochikuzhyil BM, Devi K, Fattepur SR (2010) Effect of saturated fatty acid-rich dietary vegetable oils on lipid profile, antioxidant enzymes and glucose tolerance in diabetic rats. Indian J Pharm 42(3):142–145Google Scholar
  21. Kousoulaki K, ØstbyeTK, Krasnov A, Torgersen JS (2015) Metabolism, health and fillet nutritional quality in Atlantic salmon (Salmo salar) fed diets containing n-3-rich microalgae. J Nutr Sci. 4: e24.Google Scholar
  22. Li C, Shao Y (2006) Advances in glucose transporter 4 transposition signal transduction pathways. Adv Mod Biomed Sci 6(7):54–56Google Scholar
  23. Lichtenstein AH, Schwab US (2000) Relationship of dietary fat to glucose metabolism. Atherosclerosis 150(2):227–243Google Scholar
  24. Lihn AS, Pedersen SB, Richelsen B (2010) Adiponectin: action, regulation and association to insulin sensitivity. Obes Rev 6(1):13–21Google Scholar
  25. Lu RH, Zhou Y, Yuan XC, Liang XF, Fang L, Bai XL, Wang M, Zhao YH (2015) Effects of glucose, insulin and triiodothyroxine on leptin and leptin receptor expression and the effects of leptin on activities of enzymes related to glucose metabolism in grass carp (Ctenopharyngodon idella) hepatocytes. Fish Physiol Biochem 41(4):1–9Google Scholar
  26. Mcgarry JD (1998) Glucose-fatty acid interactions in health and disease. Am J Clin Nutr 67(3 Suppl):500S–504SGoogle Scholar
  27. Michel M, Page-Mccaw PS, Chen W, Cone RD (2016) Leptin signaling regulates glucose homeostasis, but not adipostasis, in the zebrafish. Proc Natl Acad Sci U S A 113(11):3084–3089Google Scholar
  28. Ming Y (2013) Saturated fatty acid palmitate-induced insulin resistance is accompanied with myotube loss and the impaired expression of health benefit myokine genes in C2C12 myotubes. Lipids Health Dis 12(1):104–104Google Scholar
  29. Mordier S, Iynedjian PB (2007) Activation of mammalian target of rapamycin complex 1 and insulin resistance induced by palmitate in hepatocytes. Biochem Biophys Res Commun 362(1):206–211Google Scholar
  30. Moreno-Aliaga MJ, Stanhope KL, Gregoire FM, Warden CH, Havel PJ (2003) Effects of inhibiting transcription and protein synthesis on basal and insulin-stimulated leptin gene expression and leptin secretion in cultured rat adipocytes. Biochem Biophys Res Commun 307(4):907–914Google Scholar
  31. Mu H, Shen H, Liu J, Xie F, Zhang W, Mai K (2018) High level of dietary soybean oil depresses the growth and anti-oxidative capacity and induces inflammatory response in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol 77: 465-473Google Scholar
  32. Navarro I, Leibush B, Moon TW, Plisetskaya EM, Baños N, Méndez E, Planas JV, Gutiérrez J (1999) Insulin, insulin-like growth factor-I (IGF-I) and glucagon: the evolution of their receptors. Comp Biochem Physiol B Biochem Mol Biol 122(2):137–153Google Scholar
  33. Ogawa Y, Masuzaki H, Hosoda K, Aizawaabe M, Suga J, Suda M, Ebihara K, Iwai H, Matsuoka N, Satoh N (1999) Increased glucose metabolism and insulin sensitivity in transgenic skinny mice overexpressing leptin. Diabetes 48(9):1822–1829Google Scholar
  34. Okere IC, Chandler MP, Mcelfresh TA et al (2006) Differential effects of saturated and unsaturated fatty acid diets on cardiomyocyte apoptosis, adipose distribution, and serum leptin [J]. AJP Heart Circ Physiol 291(1):H38–H44Google Scholar
  35. Otukonyong EE, Dube MG, Torto R, Kalra PS, Kalra SP (2005) Central leptin differentially modulates ultradian secretory patterns of insulin, leptin and ghrelin independent of effects on food intake and body weight. Peptides 26(12):2559–2566Google Scholar
  36. Pederson T, Kramer D, Rondinone C (2001) Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes 50(1):24–31Google Scholar
  37. Piedecausa MA, Mazon MJ, Garcia GB, Hernandez MD (2007) Effects of total replacement of fish oil by vegetable oils in the diets of sharpsnout seabream (Diplodus puntazzo). Aquaculture 263(1):211–219Google Scholar
  38. Pifferi F, Jouin M, Alessandri JM, Haedke U, Roux F, Perrière N, Denis I, Lavialle M, Guesnet P (2007) n-3 fatty acids modulate brain glucose transport in endothelial cells of the blood–brain barrier. Prostaglandins Leukot Essent Fat Acids 77(5):279–286Google Scholar
  39. Reseland JE, Haugen F, Hollung K, Solvoll K, Halvorsen B, Brude IR, Nenseter MS, Christiansen EN, Drevon CA (2001) Reduction of leptin gene expression by dietary polyunsaturated fatty acids. J Lipid Res 42(5):743–750Google Scholar
  40. Roden M, Price TB, Perseghin G, Petersen KF, Rothman DL, Cline GW, Shulman GI (1996) Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Investig 97(12):2859–2865Google Scholar
  41. Rossetti L, Massillon D, Barzilai N, Vuguin P, Chen W, Hawkins M, Wu J, Wang J (1997) Short term effects of leptin on hepatic gluconeogenesis and in vivo insulin action. J Biol Chem 272(44):27758–27763Google Scholar
  42. Schmitzpeiffer C, Craig DL, Biden TJ (1999) Ceramide generation is sufficient to account for the inhibition of the insulin-stimulated PKB pathway in C2C12 skeletal muscle cells pretreated with palmitate. J Biol Chem 274(34):24202–24210Google Scholar
  43. Seufert J, Kieffer TJ, Leech CA, Holz GG, Moritz W, Ricordi C, Habener JF (1999) Leptin suppression of insulin secretion and gene expression in human pancreatic islets: implications for the development of adipogenic diabetes mellitus. J Clin Endocrinol Metab 84(2):670–676Google Scholar
  44. Sissener NH, Hemre GI, Espe M, Sanden M, Torstensen BE, Hevrøy EM (2013) Effects of plant-based diets on glucose and amino acid metabolism, leptin, ghrelin and GH-IGF system regulation in Atlantic salmon (Salmo salar L.). Aquac Nutr 19(3):399–412Google Scholar
  45. Stefan N, Fritsche A, Häring H, Stumvoll M (2001) Acute stimulation of leptin concentrations in humans during hyperglycemic hyperinsulinemia. Influence of free fatty acids and fasting. Int J Obes Relat Metab Disord 25(1):138–142Google Scholar
  46. Storlien LH, Kraegen EW, Chisholm DJ, Ford GL, Bruce DG, Pascoe WS (1987) Fish oil prevents insulin resistance induced by high-fat feeding in rats. Science 237(4817):885–888Google Scholar
  47. Stubhaug I, Tocher DR, Bell JG, Dick JR, Torstensen BE (2005) Fatty acid metabolism in Atlantic salmon (Salmo salar L.) hepatocytes and influence of dietary vegetable oil. Biochim Biophys Acta Mol Cell Biol Lipids 1734(3):277–288Google Scholar
  48. Takayuki S, Noriyasu K, Mariko TM, Koichi I, Kozo T (2013) Colonic delivery of docosahexaenoic acid improves impaired glucose tolerance via GLP-1 secretion and suppresses pancreatic islet hyperplasia in diabetic KK-A(y) mice. Int J Pharm 450(1–2):63–69Google Scholar
  49. Tan SX, Fisher-Wellman KH, Fazakerley DJ, Ng Y, Pant H, Li J, Meoli CC, Coster AC, Stöckli J, James DE (2015) Selective insulin resistance in adipocytes. J Biol Chem 290(18):11337–11348Google Scholar
  50. Tong G, Guo B, Gao Q (2002) Effects of lipid-regulating therapy on improving insulin sensitivity in patients with abnormal glucose metabolism. Chin J Clin Pharmacol 18(6):403–406Google Scholar
  51. van de Werve G, Lange A, Newgard C, Méchin MC, Li Y, Berteloot A (2010) New lessons in the regulation of glucose metabolism taught by the glucose 6-phosphatase system. FEBS J 267(6):1533–1549Google Scholar
  52. Walker CG, Bryson JM, Bell-Anderson KS, Hancock DP, Denyer GS, Caterson ID (2005) Insulin determines leptin responses during a glucose challenge in fed and fasted rats. Int J Obes 29(4):398–405Google Scholar
  53. Xu D, Xu J, Wang C, He Y (1999) Study on the relationship between plasma triglyceride level and insulin sensitivity. J Xinjiang Med Univ 1:32–34Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.The Key Laboratory of Mariculture (Ministry of Education), The Key Laboratory of Aquaculture Nutrition and Feeds (Ministry of Agriculture), Fisheries CollegeOcean University of ChinaQingdaoChina
  2. 2.Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and TechnologyQingdaoChina

Personalised recommendations